St. Petersburg Homes with a Guest House For Sale

Looking for a new home with a guest house in St. Petersburg FL? If so, you're in the right place. It's here you'll be able to break down your search and browse property listings that fit all your needs and wants perfectly. As St. Petersburg's top hyper-local website for searching available homes with a guest house, our mission is to provide home buyers just like you an easy and effective way to find the perfect new place to live! If you register on our website, we can also send you disclosures, past sales history, dates and prices of homes recently sold nearby, and also all of the latest property listings that match your search criteria to hit the market, allowing you to stay one-step ahead of other St. Petersburg home buyers. 

To get your search started, simply start browsing all of the available St. Petersburg homes with a guest house below, and if you have any questions about a particular property or would even like to take that next step and schedule a home tour, call or text us at (813) 817-0345 now! 

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$15,100,000

2000 Park Street N, ST PETERSBURG

5 Beds 6 Baths 10,395 SqFt Residential MLS® # TB8495795

$12,500,000

416 Brightwaters Boulevard Ne, ST PETERSBURG

5 Beds 6 Baths 6,065 SqFt Residential MLS® # TB8491058

$11,000,000

↓ $500,000

1571 Oceanview Drive, ST PETERSBURG

7 Beds 11 Baths 12,046 SqFt Residential MLS® # TB8336934

$7,600,000

↓ $350,000

5237 61st Avenue S, ST PETERSBURG

4 Beds 5 Baths 4,511 SqFt Residential MLS® # TB8432616

$6,999,000

106 2nd Avenue, ST PETE BEACH

5 Beds 6 Baths 4,724 SqFt Residential MLS® # TB8426239

$5,995,000

↓ $500,000

337 Coffee Pot Drive Ne, ST PETERSBURG

5 Beds 6 Baths 6,239 SqFt Residential MLS® # TB8496270

Pending

$5,750,000

↓ $245,000

6199 54th Street S, ST PETERSBURG

5 Beds 6 Baths 6,147 SqFt Residential MLS® # TB8439000

$5,590,000

↓ $60,000

1365 Brightwaters Boulevard Ne, ST PETERSBURG

5 Beds 5 Baths 6,060 SqFt Residential MLS® # TB8412312

$5,420,069

↓ $274,131

5405 Leilani Drive, ST PETE BEACH

5 Beds 6 Baths 5,213 SqFt Residential MLS® # TB8418141

$5,345,000

2051 Illinois Avenue Ne, ST PETERSBURG

5 Beds 7 Baths 5,712 SqFt Residential MLS® # TB8533168

$4,950,000

6043 Bayou Grande Boulevard Ne, ST PETERSBURG

5 Beds 5 Baths 5,793 SqFt Residential MLS® # TB8511030

$4,855,000

↓ $20,000

2121 Bayou Grande Boulevard Ne, ST PETERSBURG

5 Beds 7 Baths 5,812 SqFt Residential MLS® # U8253104

$4,500,000

↓ $250,000

5212 62nd Avenue S, ST PETERSBURG

6 Beds 7 Baths 6,424 SqFt Residential MLS® # TB8472517

$4,455,000

↓ $20,000

838 Monterey Boulevard Ne, ST PETERSBURG

5 Beds 5 Baths 4,334 SqFt Residential MLS® # TB8452164

$4,425,000

874 Placido Way Ne, ST PETERSBURG

4 Beds 4 Baths 3,622 SqFt Residential MLS® # TB8510443

$4,395,000

3830 Shore Acres Boulevard Ne, ST PETERSBURG

6 Beds 7 Baths 5,186 SqFt Residential MLS® # TB8472930

$4,100,000

4635 Dolphin Cay Lane S, ST PETERSBURG

3 Beds 4 Baths 3,647 SqFt Residential MLS® # TB8467613

$3,995,000

601 Cordova Boulevard Ne, ST PETERSBURG

5 Beds 6 Baths 4,325 SqFt Residential MLS® # TB8522019

$3,925,000

↓ $200,000

841 Ponce De Leon Drive, ST PETERSBURG

5 Beds 7 Baths 6,512 SqFt Residential MLS® # TB8392286

$3,900,000

1803 Beach Drive Se, ST PETERSBURG

5 Beds 7 Baths 4,790 SqFt Residential MLS® # TB8494837

$3,749,000

↓ $251,000

5264 61st Avenue S, ST PETERSBURG

4 Beds 5 Baths 6,367 SqFt Residential MLS® # TB8477321

$3,695,000

456 Rafael Boulevard Ne, ST PETERSBURG

5 Beds 6 Baths 5,206 SqFt Residential MLS® # TB8531868

$3,599,000

↓ $100,000

482 Hermosita Drive, ST PETE BEACH

6 Beds 6 Baths 5,206 SqFt Residential MLS® # TB8465360

Pending

$3,500,000

1200 Friendly Way S, ST PETERSBURG

6 Beds 6 Baths 5,143 SqFt Residential MLS® # TB8525687

Pending

$3,250,000

↓ $125,000

4401 38th Street S, ST PETERSBURG

4 Beds 6 Baths 4,044 SqFt Residential MLS® # TB8465602

$3,250,000

2038 Carolina Avenue Ne, ST PETERSBURG

4 Beds 3 Baths 3,109 SqFt Residential MLS® # TB8516990

Pending

$3,000,000

1846 Coffee Pot Boulevard Ne, ST PETERSBURG

4 Beds 3 Baths 2,997 SqFt Residential MLS® # TB8519019

$2,880,000

↓ $115,000

1976 Kansas Avenue Ne, ST PETERSBURG

5 Beds 6 Baths 4,757 SqFt Residential MLS® # TB8453291

Pending

$2,798,000

↓ $192,000

356 Belleair Drive Ne, ST PETERSBURG

4 Beds 5 Baths 4,267 SqFt Residential MLS® # TB8500020

$2,788,000

732 And 732 1/2 Ne Oak Street, ST PETERSBURG

6 Beds 5 Baths 4,608 SqFt Residential MLS® # TB8513524

$2,595,000

3896 42nd Avenue S, ST PETERSBURG

3 Beds 3 Baths 2,957 SqFt Residential MLS® # TB8531236

Openhouse

$2,575,000

↓ $75,000

1100 Friendly Way S, ST PETERSBURG

5 Beds 4 Baths 4,283 SqFt Residential MLS® # TB8432607

New Listing

$2,500,000

1946 Illinois Avenue Ne, ST PETERSBURG

4 Beds 4 Baths 3,198 SqFt Residential MLS® # TB8537945

Pending

$2,499,000

↓ $50,000

151 Punta Vista Drive, ST PETE BEACH

3 Beds 3 Baths 2,182 SqFt Residential MLS® # TB8496807

Pending

$2,495,000

↓ $200,000

1815 Bayou Grande Boulevard Ne, ST PETERSBURG

4 Beds 4 Baths 4,456 SqFt Residential MLS® # TB8460108

$2,495,000

113 7th Street E, ST PETERSBURG

4 Beds 5 Baths 4,350 SqFt Residential MLS® # TB8531097

Pending

$2,490,000

↓ $100,000

850 59th Avenue, ST PETE BEACH

4 Beds 4 Baths 2,900 SqFt Residential MLS® # TB8404528

$2,399,000

1001 Cordova Boulevard Ne, ST PETERSBURG

5 Beds 5 Baths 3,917 SqFt Residential MLS® # TB8505011

$2,399,000

↓ $51,000

151 17th Avenue N, ST PETERSBURG

5 Beds 4 Baths 3,509 SqFt Residential MLS® # TB8505601

$2,395,000

↓ $100,000

6062 Bayou Grande Boulevard Ne, ST PETERSBURG

5 Beds 7 Baths 5,122 SqFt Residential MLS® # TB8467428

Pending

$2,295,000

1230 Darlington Oak Circle Ne, ST PETERSBURG

5 Beds 5 Baths 4,254 SqFt Residential MLS® # TB8518629

Pending

$2,200,000

↓ $295,000

4603 Osprey Drive S, ST PETERSBURG

5 Beds 5 Baths 2,753 SqFt Residential MLS® # TB8418745

$2,195,000

↓ $54,000

220 90th Avenue Ne, ST PETERSBURG

4 Beds 4 Baths 3,673 SqFt Residential MLS® # TB8523597

Pending

$2,190,000

↓ $85,000

1710 Brightwaters Boulevard Ne, ST PETERSBURG

4 Beds 3 Baths 3,992 SqFt Residential MLS® # TB8471809

$2,165,000

↓ $10,000

911 Jungle Avenue N, ST PETERSBURG

5 Beds 5 Baths 4,106 SqFt Residential MLS® # O6358654

$2,150,000

4935 62nd Avenue S, ST PETERSBURG

4 Beds 3 Baths 3,104 SqFt Residential MLS® # TB8459428

Pending

$2,150,000

4333 10th Street N, ST PETERSBURG

5 Beds 4 Baths 3,576 SqFt Residential MLS® # TB8466075

$2,150,000

436 12th Avenue Ne, ST PETERSBURG

5 Beds 5 Baths 3,136 SqFt Residential MLS® # TB8502922

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Continue Searching Homes with a Guest House in Florida 

Not seeing the right home with a guest house that fits your needs, wants, or budget here? Continue searching homes for sale with a guest house for sale in other Florida cities and towns using our homes with a guest house-by-city directory below. 

Buying a Home with a Guest House in St. Petersburg, FL  

St. Petersburg, FL, known for its stunning waterfronts and thriving arts community, is quickly becoming a top destination for homebuyers seeking properties with guest houses. The growing popularity of homes with additional living spaces in this vibrant city reflects modern trends in home functionality, while also taking advantage of its unique local appeal.

Why Guest Houses Are Gaining Popularity  

Homes with guest houses offer unmatched versatility. They provide extra space for accommodating family members, particularly for multi-generational households. This is especially attractive in St. Petersburg, where the warm climate and picturesque surroundings draw many retirees eager to be close to loved ones. Guest houses also offer privacy for visitors, enhancing their stay in this bustling yet scenic city.  

Another key driver is the potential for rental income. St. Petersburg, with its world-class beaches, renowned museums such as The Dalí, and lively events like the Saturday Morning Market, attracts a steady stream of tourists year-round. Properties with guest houses can be ideal for short-term rentals, giving homeowners the opportunity to generate income while leveraging the city’s booming tourism industry.  

St. Petersburg-Specific Appeal  

With its warm, sunny weather and pedestrian-friendly neighborhoods, St. Petersburg provides an ideal backdrop for properties with guest houses. Many of these homes are located in charming areas near attractions like the Central Arts District or along the waterfront, where guest houses are especially sought-after for their potential to accommodate both locals and visitors. Additionally, as the city sees an influx of people relocating from northern states, buyers are actively seeking residences that blend practicality with Florida’s renowned laid-back lifestyle.  

Buying a home with a guest house in St. Petersburg is more than a real estate purchase—it’s an investment in flexibility, lifestyle, and future earning potential, all set against the backdrop of one of Florida’s most exciting and culture-filled cities. 

St. Petersburg Realtors Specializing in Homes With a Guest House

If you are thinking about buying or selling a home in St. Petersburg with a guest house, our team can help you navigate the current housing landscape and get you the best possible price based on current market conditions. Simply put, we know the St. Petersburg real estate market better than anyone!

Contact Mike + Michelle to see why our expertise working with St. Petersburg homes with a guest house helps makes us the perfect fit for all your home buying and selling needs. And in the meantime, also continue searching other homes for sale in the area using our Advanced Search.